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Environmental and Plant Genetic Factors Influencing Phyllosphere

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Environmental and Plant Genetic Factors Influencing Phyllosphere University of Warwick institutional repository: http://go.warwick.ac.uk/wrap This paper is made available online in accordance with publisher policies. Please scroll down to view the document itself. Please refer to the repository record for this item and our policy information available from the repository home page for further information. To see the final version of this paper please visit the publisher’s website. Access to the published version may require a subscription. Author(s): Whipps, J.M.; Hand, P.; Pink, D.; Bending, G.D. Article Title: Phyllosphere microbiology with special reference to diversity and plant genotype Year of publication: 2008 Link to published version: http://dx.doi.org/10.1111/j.1365- 2672.2008.03906.x Publisher statement: The definitive version is available at www.blackwell-synergy.com 1 Phyllosphere microbiology with special reference to diversity and plant 2 genotype 3 John M. Whipps, Paul Hand, David Pink and Gary D. Bending 4 Warwick HRI, University of Warwick, Wellesbourne, Warwick CV35 9EF, UK 5 6 Summary 7 The phyllosphere represents the habitat provided by the aboveground parts of plants, and on a 8 global scale supports a large and complex microbial community. Microbial interactions in the 9 phyllosphere can affect the fitness of plants in natural communities, the productivity of 10 agricultural crops, and the safety of horticultural produce for human consumption. The 11 structure of phyllosphere communities reflects immigration, survival and growth of microbial 12 colonists, which is influenced by numerous environmental factors in addition to leaf physico- 13 chemical properties. The recent use of culture independent techniques has demonstrated 14 considerable previously unrecognised diversity in phyllosphere bacterial communities. Deleted: significant 15 Furthermore there is significant recent evidence that plant genotype can play a major role in 16 determining the structure of phyllosphere microbial communities. The main aims of this 17 review are (i) to discuss the diversity of phyllosphere microbial populations (ii) to consider 18 the processes by which microbes colonise the phyllosphere (iii) to address the leaf 19 characteristics and environmental factors which determine survival and growth of colonists Deleted: to 20 (iv) to discuss microbial adaptations which allow establishment in the phyllosphere habitat 21 and (v) to evaluate evidence for plant genotypic control of phyllosphere communities. Finally, 22 we suggest approaches and priority areas for future research on phyllosphere microbiology. 23 24 Keywords: phyllosphere, bacteria, fungi, diversity, culture-independent profiling, plant 25 genotype 1 1 2 Introduction 3 The aerial parts of living plants including leaves, stems, buds, flowers and fruits provide a 4 habitat for microorganisms termed the phyllosphere. Bacteria are considered to be the 5 dominant microbial inhabitants of the phyllosphere, although archaea, filamentous fungi, and 6 yeasts may also be important. These microbes can be found both as epiphytes on the plant 7 surface and as endophytes within plant tissues (Arnold, et al. 2000; Inacio et al. 2002; Lindow 8 and Brandl 2003; Stapleton and Simmons 2006). The global surface area of the phyllosphere 9 has been estimated to total over 4 x 108 km2, supporting bacterial populations in the region of 10 1026 cells (Morris and Kinkel 2002). Furthermore, recent estimates of the diversity of 11 phyllosphere bacteria in the 20 000 vascular plants inhabiting the Brazillian Atlantic forest, 12 suggests the possible occurrence of 2 to 13 million phyllosphere bacterial species in this 13 habitat alone (Lambais et al. 2006). 14 The phyllosphere represents a niche with great agricultural and environmental 15 significance. There is growing evidence for important interactions of phyllosphere microbial 16 inhabitants which may affect the fitness of natural plant populations and the quality and 17 productivity of agricultural crops. Phyllosphere bacteria can promote plant growth and both 18 suppress and stimulate the colonisation and infection of tissues by plant pathogens (Lindow 19 and Brandl 2003; Rasche et al., 2006). Similarly, fungal endophytes of leaves may deter 20 herbivores, protect against pathogens and increase drought tolerance (Arnold et al. 2003; 21 Schweitzer et al. 2006). Furthermore, interactions in the phyllosphere zone determine the 22 extent to which human pathogens are able to colonise and survive on plant tissues, an area of 23 increasing importance with the rise in cases of human disease associated with consumption of Deleted: 2006 24 fresh salad, fruit and vegetable produce (Whipps et al. 2008). 2 1 There is evidence for functional roles within the phyllosphere microbial community which 2 given the size of the habitat could have global significance. The best studied of these is 3 nitrogen fixation. Measured rates of bacterial nitrogen fixation in the phyllosphere vary 4 widely, but in the phyllosphere of trees in some tropical habitats has been reported at rates of 5 over 60 kg N ha-1, although amounts fixed in the phyllosphere of temperate trees is generally 6 considerably lower (Freiberg 1998). Furthermore, N2 fixation or the presence of N2 fixing 7 bacteria has been reported in the phyllosphere of many crop plants (e.g. Murty 1983; 8 Miyamoto et al. 2004). Other environmentally important microbial processes for which there 9 is evidence in the phyllosphere include methanol degradation (Corpe and Rheem, 1989; Van 10 Aken et al. 2004) and nitrification (Papen et al. 2002), although the rates of these process and 11 their ubiquity within the phyllosphere remains to be elucidated. 12 Most knowledge of the structure and activities of phyllosphere microbial communities has 13 been established using culture-dependant methods. However, these are recognised to 14 significantly underestimate diversity, with only 0.1-3 % of environmental bacteria considered 15 culturable (Wagner et al. 1993). Data gathered using these methods therefore relate only to 16 culturable members of the community and provide no information on the vast majority of 17 microbes present in samples. As in other areas of environmental microbiology, the recent 18 application of culture-independent methods based on the characterisation of small subunit 19 rRNA gene sequences for microbial community analysis is providing new insights into the 20 complexity of phyllosphere microbial communities and their interactions with plants and the 21 wider environment. Deleted: The main aims of this review 22 In the current paper we review the extent to which the use of culture independent Deleted: are 23 approaches has changed our understanding of the structure and diversity of phyllosphere 24 communities. A variety of plant, microbial and environmental factors control establishment of 25 microbial communities in the phyllosphere, but recently there has been recognition of the role 3 1 that plant genotype plays in selecting phyllosphere communities. The evidence for the 2 different factors which regulate the structure of phyllosphere communities is discussed with Deleted: (i) to discuss the diversity of phyllosphere 3 special reference to the role of plant genotype. Finally, we suggest approaches and priority microbial populations (ii) to consider the processes by which microbes colonise the 4 areas for future research on phyllosphere microbiology. Although much of the phyllosphere phyllosphere (iii) to address the leaf characteristics and environmental factors which 5 literature is concerned with interactions between plant and plant pathogens (bacteria and fungi determine survival and growth of colonists (iv) to discuss microbial adaptations to the phyllosphere 6 that cause diseases in plants), in the current review emphasis is placed on studies of habitat and (v) to evaluate evidence for plant genotypic control of phyllosphere 7 microorganisms that live in the phyllosphere without causing obvious damage to the plant, as communities. Deleted: Particular attention 8 absence of disease is the normal situation in nature. will be given to recent advances in understanding gained through the application of culture 9 independent methods. 10 Microbial diversity in the phyllosphere 11 The microbial communities of the phyllosphere are diverse, supporting numerous genera of 12 bacteria, filamentous fungi, yeasts, algae and in some situations protozoans and nematodes 13 (Morris et al. 2002; Lindow and Brandl 2003). Bacteria are the most numerous and diverse 14 colonists of leaves, with culturable counts ranging between 102 to 1012 cells g leaf (Thompson 15 et al. 1993; Inacio et al. 2002). Culture-based studies of sugar beet over the whole of the 16 growing season have found more than 78 bacterial species representing 37 known bacterial 17 genera (Thompson et al. 1993). Similar studies in wheat have revealed 88 bacterial species Deleted: However, r 18 representing 37 known bacterial genera (Legard et al. 1994). 19 Recent studies have demonstrated that profiling of phyllosphere communities based on Deleted: in 20 culture dependent methods is likely to be inaccurate and to underestimate diversity (Rasche et Deleted: 21 al. 2006b). In the case of the phyllosphere, use of culture independent approaches has shown 22 that although assumptions regarding the dominant inhabitants are largely correct, the diversity Deleted: ¶ 23 of phyllosphere communities is far greater than previously recognised.Analysis of 16S rDNA 24 cloned directly from leaf samples has demonstrated
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